Perceptuo-motor planning during functional reaching after stroke

In healthy young adults, reaching movements are planned such that the initial grasp position on the object is modulated based on the final task goal. This perceptuo-motor coupling has been described as the end-state comfort effect. This study aimed to determine the extent to which visuo-perceptual and motor deficits, but not neglect, due to stroke impact end-state comfort measured as the grasp-height effect. Thirty-four older adults (17 controls, 17 chronic stroke) performed a functional goal-directed two-sequence task with each arm, consisting of reaching and moving a cylindrical object (drain plunger) from an initial to four target platform heights, standardized to body height, in a block randomized sequence. Arm motor impairment (Fugl-Meyer Assessment) and visual–perceptual deficits (Motor-Free Visual Perception Test) were assessed in stroke subjects, and arm and trunk kinematics were assessed in all subjects. The primary outcome measure of the grasp-height effect was the relationship between the grasp heights used at the home position and the final target platform heights. Mixed model analysis was used for data analysis. The grasp-height effect was present in all participants, but decreased in stroke subjects with visuo-perceptual impairments compared to controls. In stroke subjects with sensorimotor impairments alone, indicated by altered kinematics, the grasp-height effect was comparable to controls. This first study examining the grasp-height effect in individuals with stroke provides new knowledge of the impact of visuo-perceptual deficits on movement planning and execution, which may assist clinicians in selecting more effective treatment strategies to improve perceptuo-motor skills and enhance motor recovery.

Perceptuo-motor planning during functional reaching after stroke

Perceptuo‑motor planning during functional reaching after stroke
Margit Alt Murphy 0 1 2
Melanie C. Baniña 0 1 2
Mindy F. Levin 0 1 2
0 Center for Interdisciplinary Research in Rehabilitation (CRIR), McGill University , Montreal, QC , Canada
1 School of Physical and Occupational Therapy, McGill University , Montreal, QC , Canada
2 Institute of Neuroscience and Physiology, Rehabilitation Medicine, Sahlgrenska Academy, University of Gothenburg , Per Dubbsgatan 14, Plan 3, 41345 Gothenburg , Sweden
3 Margit Alt Murphy
In healthy young adults, reaching movements are planned such that the initial grasp position on the object is modulated based on the final task goal. This perceptuomotor coupling has been described as the end-state comfort effect. This study aimed to determine the extent to which visuo-perceptual and motor deficits, but not neglect, due to stroke impact end-state comfort measured as the graspheight effect. Thirty-four older adults (17 controls, 17 chronic stroke) performed a functional goal-directed twosequence task with each arm, consisting of reaching and moving a cylindrical object (drain plunger) from an initial to four target platform heights, standardized to body height, in a block randomized sequence. Arm motor impairment (Fugl-Meyer Assessment) and visual-perceptual deficits (Motor-Free Visual Perception Test) were assessed in stroke subjects, and arm and trunk kinematics were assessed in all subjects. The primary outcome measure of the grasp-height effect was the relationship between the grasp heights used at the home position and the final target platform heights. Mixed model analysis was used for data analysis. The graspheight effect was present in all participants, but decreased in stroke subjects with visuo-perceptual impairments compared to controls. In stroke subjects with sensorimotor impairments alone, indicated by altered kinematics, the grasp-height effect was comparable to controls. This first study examining the grasp-height effect in individuals with stroke provides new knowledge of the impact of visuo-perceptual deficits on movement planning and execution, which may assist clinicians in selecting more effective treatment strategies to improve perceptuo-motor skills and enhance motor recovery.
End-state comfort effect; Arm; Kinematics; Stroke; Anticipatory motor planning; Visual perception
Introduction
Movements of the upper limb during daily activities are
complex and require the coordination between multiple
muscles, joints and body segments in close interaction with
environmental and personal constraints
(Gibson 2015; Greeno
1994; Shumway-Cook and Woollacott 2012)
. Visual input,
perception and cognitive processing of available information
in the environment are involved in the formation of an action
plan appropriate for the task
(Marteniuk et al. 1987)
.
Several motor control models based on dynamical systems and
ecological theory have been proposed to explain different
aspects of movement planning and execution of multijoint
functional tasks. These models emphasize the importance
of the interaction between the individual, environment and
task, and explain movements through optimization
principles, such as minimizing the degrees of freedom, avoiding
biomechanical discomfort or prioritizing comfortable final
arm or hand postures
(Gielen 2009; Jeannerod et al. 1998;
Latash 2012; Rosenbaum et al. 2006; Solnik et al. 2013;
Turvey and Fonseca 2009)
.
Contextual constraints, such as object properties, object
location with respect to the body and the goal of the task,
impact motor planning and execution
(Jeannerod et al. 1998;
Marteniuk et al. 1987; Turvey and Fonseca 2009)
. For
example, the kinematics of a pointing task differ from reaching
and grasping tasks, in the same way as a reaching movement
differs depending on whether a simulated or real object is
used
(Armbruster and Spijkers 2006; Grafton et al. 1996;
Marteniuk et al. 1987)
. Arm, hand and fingers during
reaching are positioned in a way that is sensitive to the location,
size, and orientation of the object, but also to how the object
will be used, e.g., object affordance
(Cohen and Rosenbaum
2004; Jeannerod et al. 1998; Rosenbaum et al. 2009)
.
One way to study movement planning and
perceptuomotor coupling is by using tasks in which the end-state
comfort is manipulated
(Rosenbaum et al. 1990)
. The end-state
comfort effect is the tendency of the sensorimotor system
to prioritize a comfortable hand and arm position at the end
of an object manipulation task rather than at the beginning
(Rosenbaum et al. 2012)
. For example, when young adults
were asked to grasp and move an object with a vertical shaft
(drain plunger) from its initial position on one platform to a
target platform of a different height, they grasped the shaft
lower when the plunger was to be moved to higher shelves
and higher to move the plunger to lower shelves
(Cohen and
Rosenbaum 2004)
. The preferred grasp height was linearly
related to the target platform height onto which the object
was to be moved, called the grasp-height effect. The authors
concluded that young healthy adults planned movements
beyond the first phase of the task and that end-state comfort
was usually prioritized over initial-state comfort
(Cohen and
Rosenbaum 2004)
. Although other tasks requiring
positioning of the hand throughout a 180 degree continuous task
space may be more sensitive to study perceptuo-motor
coupling
(Wunsch et al. 2013)
, these tasks may also require a
higher level of motor ability. Thus, in this first study of
individuals with stroke, we chose to study the end-state comfort
effect of grasp height. The end-state comfort effect is
reliably present only beyond the age of 9–10 years
(Stockel et al.
2012; Wunsch et al. 2013)
and declines with increasing age,
which may be associated with reduced cognitive
capabilities (Wunsch et al. 2015). Studies investigating the end-state
comfort effect in adult clinical populations are few
(Rosenbaum et al. 2012; Tan et al. 2012)
and how perceptuo-motor
coupling may be affected by stroke has not been addressed.
After stroke, several body functions influencing daily
activities and consequently participation in social life may be
impaired
(Beaudoin et al. 2013; Hochstenbach et al. 1998)
.
In addition to commonly reported sensorimotor and
cognitive impairments, visual perception is impaired in
approximately 30–50% of persons
(Beaudoin et al. 2013; Nys et al.
2007)
. Visuo-perceptual deficits have also been linked to
restrictions in activities and participation in daily life
(Beaudoin et al. 2013; Titus et al. 1991)
. Visuo-perceptual deficits
differ from visuospatial neglect that is a disorder of attention
and awareness primarily resulting from right-sided brain
lesions (Proto et al. 2009). Visuospatial neglect influences
motor planning and subsequent movement execution
(Peters
et al. 2015)
and may therefore mask more subtle and often
non-diagnosed visuo-perceptual deficits
(Hermsdorfer et al.
1999)
.
The design of the study was based on the ecological
theory originating from psychology emphasizing that
perception of object affordances together with the goal of the
task impact motor planning and execution
(Gibson 2015;
Randerath and Frey 2015; Rosenbaum et al. 2012)
. Since a
large proportion of patients may have non-neglect
perceptual deficits after stroke
(Proto et al. 2009)
that may
influence motor learning capacity, valuable information can be
obtained by investigating how these deficits affect
anticipatory motor planning and movement execution. This
knowledge may guide clinicians in the selection of interventions
to improve perceptuo-motor skills related to reaching and
grasping and enhance upper limb recovery. Thus, the aim
of this study was to determine to what extent non-neglect
visuo-perceptual deficits and motor deficits in persons with
stroke impact prospective motor planning determined by the
grasp-height effect in reaches to different target heights.
Our first hypothesis was that the grasp-height effect
would be decreased in persons with stroke who have
visuoperceptual deficits, compared to healthy controls and to
individuals with stroke without visuo-perceptual impairments.
Since perceptual deficits would impact both arms, the effect
of these deficits would be most clearly observable when the
task is performed with the non-paretic arm as movements of
this arm would not be confounded by concurrent motor
deficits. Our second hypothesis was that the grasp-height effect
would be decreased in persons with stroke who have motor
deficits in the paretic arm compared to healthy controls.
Motor deficits may limit the choice of grasp location because
of limitations in the ability to reach, orient the hand for
grasping and to use different types of grasps
(Roby-Brami
et al. 2003)
. We anticipated that the effect of motor
impairment alone would be most evident in paretic arm of persons
without visuo-perceptual deficits. Preliminary results have
appeared in abstract form
(Alt Murphy and Levin 2016)
.
Methods
Subjects
Seventeen persons with chronic stroke and 17 healthy
controls (8 male, mean age 63.7 ± 12.0 years, range
40–78 years) participated. Inclusion criteria for
participants with stroke were: presence of unilateral stroke at
least 6 months earlier defined according to World Health
Organization criteria by imaging or clinical assessment;
age between 40 and 80 years; presence of impaired upper
limb function (Chedoke McMaster Stroke Assessment
Arm and Hand sections ≥4/7); ability to grasp and lift
a cylindrical object with the affected arm above
shoulder height without pain while standing independently.
Participants were excluded if they had unilateral neglect
detected by the line bisection test
(Menon and
KornerBitensky 2004)
and/or Apples test
(Bickerton et al. 2011)
or showed signs of apraxia during clinical assessments.
Participants were also excluded if they were unable to
follow instructions in English and/or French; had other
neurological or musculoskeletal conditions affecting upper
limb reaching and grasping; or had uncorrected visual
acuity problems. Healthy controls were included if they
were between 40 and 80 years old. They were excluded
according to the same criteria as for individuals with
stroke and if they scored <31 out of 36 points on the
Motor-Free Visual Perception Test, MVPT
(Colarusso
and Hammill 2003)
. Participants were recruited through
four local rehabilitation hospital discharge lists and tested
at the Research Center of the Jewish Rehabilitation
Hospital. All participants provided written informed consent
and the study protocol was approved by the Centre for
Interdisciplinary Research in Rehabilitation of Greater
Montreal (CRIR).
Clinical evaluation
Upper limb sensorimotor impairment in participants with
stroke was assessed using the Fugl-Meyer Assessment for
Upper Extremity (FMA-UE, motor 0–66; sensation 0–12)
(Duncan et al. 1983; Fugl-Meyer et al. 1975)
. Spasticity
was assessed with the Composite Spasticity Index (0–16)
that measures both phasic and tonic stretch reflex
activity of the elbow and wrist on which a score of 4 indicates
a normal response (Levin and Hui-Chan 1993). A score
<26 out of 30 points on the Montreal Cognitive
Assessment (MoCA) indicated cognitive impairment
(Nasreddine
et al. 2005)
.
Visuo-perceptual deficits were evaluated with the
original version of the MVPT, which measures general visual
perception independently of motor ability and
discriminates between individuals with and without visual
perceptual deficits
(Cate and Richards 2000; Mazer et al. 1998)
.
The MVPT assesses visual domains of discrimination,
figure–ground discrimination, memory, completion of
fragmented pictures and spatial relations and has a
maximal score of 36. Participants with stroke were stratified
according to the presence (≤30 points, n = 7) or absence
(≥31 points, n = 10) of a visuo-perceptual impairment
(Mazer et al. 1998). All clinical assessments were
performed by an experienced physiotherapist.
Research setup and procedure
We used a perceptual motor task similar to that described
by
Cohen and Rosenbaum (2004)
that incorporated
reaching, grasping and moving an object with a vertical wooden
shaft (drain plunger, 300 g, 42 cm long 2 cm diameter) from
a “home” location in front of the contralateral arm of the
participant to four target platforms (23 × 23 cm) of different
heights in the ipsilateral arm workspace (Fig. 1). The rigid
rubber plunger base was 16 cm wide and 7 cm high. The
reach-to-move task was tested on both arms.
To be able to compare results from people of different
heights and to ensure that reaching extent was similar in all
subjects, the locations of the home and target platforms were
adjusted to body height, arm length and shoulder width of
each participant. The fixed home platform was anterior to
the contralateral shoulder at 50% of body height at a
distance of 75% arm length. Arm length was defined as the
distance between the mid-acromion to the tip of the third
finger with the shoulder at 90° and the elbow, wrist and the
fingers extended. Target platforms were located laterally to
the home platform, anterior to the ipsilateral shoulder, at
four different heights set at 35, 50, 70 and 80% of body
height.
In the initial position, participants stood with their arm
alongside their body. After a verbal “go” command, they
reached to grasp the plunger and move it from the home
platform to a selected target platform at a comfortable
selfselected speed. Participants were asked to complete the task
as naturally as possible using a whole hand (palmer) grasp.
No other instructions were given. To perform the task, the
plunger had to be grasped at some point on the vertical
shaft above the rubber base. The highest target was placed
so that the subject had to lift the plunger by extending their
arm above shoulder level. The lowest target was placed at
a level where it was possible to move the plunger without
flexing hips or knees. Thus, targets were placed within the
full range of shoulder positions. After each trial, the plunger
was brought back to the home platform by the examiner, who
grasped the base of the plunger with both hands to avoid any
observational learning effect. The procedure was repeated in
blocks of 10 trials per target with the order of target height
and starting side randomized across subjects. Prior to each
block, participants performed one practice trial before data
capture to ensure that they had understood the instructions
and were able to reach the target platform. In total, 40 trials
(4 × 10) were recorded for each arm and the entire testing
session took approximately 90 min including rest periods.
Kinematic analysis
A 3D optical motion tracking system was used to sample
data at 120 Hz (6-camera Optotrak Certus Motion Capture
System, Northern Digital Corp., Waterloo, ON, Canada).
Ten active markers (infrared emitting diodes) were placed on
the tested hand (third metacarpal head), wrist (ulnar styloid
process), elbow (lateral epicondyle), right and left shoulder
(anterior–superior acromion), thorax (mid-sternum), and
right and left ASIS. Two additional markers were placed on
the base of the plunger. In addition, a rigid body with three
markers was placed on the upper 1/3rd of the sternum to
track 3D trunk movement. NDI First Principles™ software
was used for data collection and management.
Kinematic data were analyzed using custom-made
Matlab software
(Matlab R2013b, The Mathworks Inc, Natick,
CA, USA)
and filtered using a 10-Hz low-pass Wiener filter
which accurately preserves the timing and shape of the
signal
(Wiener 1970)
. Since the task goal influences the
movement kinematics
(Marteniuk et al. 1987)
, we asked subjects
to grasp the plunger at the home position and move it to the
target platform as a continuous gesture. However, only the
first reach-to-grasp movement, from the initial position to
the time of grasping of the plunger, was analyzed. Movement
beginning and end were defined as the times at which the
tangential velocity of the hand marker exceeded or was less
than 5% of the maximal velocity for at least 50 ms.
Movement time and peak hand tangential velocity were calculated.
Arm and trunk kinematics were characterized by shoulder
horizontal adduction/abduction, elbow flexion/extension,
and axial trunk rotation angles obtained at the end of the
reach phase. Shoulder horizontal adduction was measured
as a positive angle of the vector between the acromion and
elbow markers projected horizontally and defined as 0°
when the arm was abducted laterally in line with the
shoulders. Elbow angle was determined by the angle between the
vectors joining the shoulder/elbow and elbow/wrist markers
with full extension defined as 0°.
To perform the task correctly, the individual had to choose
the height of the initial hand placement on the plunger so
that the hand position when the plunger was moved to the
final target height would be both effective and comfortable.
Thus, the presence of a grasp-height effect was defined as
a linear relationship between the grasp heights used at the
home position and the final target platform heights. A higher
grasp at the home position was expected for moves to lower
target heights, and a grasp closer to the base of the plunger
at the home position was expected for moves to higher target
heights. Initial grasp height was calculated as the vertical
distance in mm from the marker located on the base of the
plunger to the hand marker.
Statistical analysis
The SPSS (Statistical Package for Social Sciences, version
22) was used for independent t tests and Chi-square tests
to determine differences in age and sex between stroke and
healthy groups, respectively. Differences in clinical
characteristics (motor, sensation, spasticity, cognition) in the
subgroups of stroke subjects with and without visuo-perceptual
impairments were determined using Mann–Whitney U tests.
Comparisons between kinematics of the right and left arms
of healthy controls were done with paired-sample t tests or
Wilcoxon’s signed rank tests (in case of non-normal
distribution). Differences in kinematics between individuals
with stroke and healthy controls (left arm) were investigated
with one-way analyses of variance (ANOVA) with criterion
of significance of p < 0.05. Three different analyses were
performed comparing three groups at a time: (1) controls
and the affected and less-affected arm of individuals with
stroke; (2) controls and the stroke subgroups (with and
without visuo-perceptual impairment) for movements made with
the more-affected arm; (3) controls and the same stroke
subgroups for movements made with less-affected arms. Post
hoc comparisons using the Bonferroni corrections were
used.
A split-plot design was used for the analyses to
determine the effect of target platform height on initial grasp
height (dependent variable) on the plunger across
different groups. Subjects were considered as main plots and
target heights as subplots, since the order of target heights
was randomized for each subject. The groups and target
heights were considered as fixed factors and the subjects as
random factors. Interaction terms between all factors were
included in the model. The model was adjusted for age,
sex and trial order and the estimates and F values were
compared with an unadjusted model. For the stroke group,
the influence of cognitive impairment and lesion side on
the effect of target height on grasp height was evaluated
within the mixed models analysis. The mixed
SAS-procedure (Proc Mixed, SAS Institute Inc., Cary, NC, USA,
version 9.3) with restricted maximum likelihood (RELM)
estimation method was used. The RELM is recommended
for split-plot designs as it yields good results for various
relative magnitudes of the variance components even with
small and second-order designs
(Goos 2006; Kenward and
Roger 1997)
. The assumptions for the analyses were
verified by residual plots of predicted values, histograms and
q–q plots.
To verify whether the grasp-height effect was decreased
in persons with stroke compared to controls, group and
interaction effects between group and target height were
investigated. Absolute grasp heights for each target height
condition as well as the pairwise grasp height differences
(within groups) across target platform heights were
calculated and compared between controls and subjects with
stroke. The grasp height differences in subjects with stroke
were compared to controls in a piecewise linear analysis
between each pair of target height condition. In addition,
grasp height differences (within groups) between each pair
of adjacent targets were compared to no (zero) difference.
Subsequently, pairwise slopes of grasp heights between
the low and high target platform heights were plotted to
verify whether the grasp-height effect was decreased in
stroke subjects compared to controls. In all comparisons
of grasp heights, a Bonferroni p value correction was used
(p < 0.025) to correct for testing the two arms (affected
and less-affected) in the whole group analysis; and the two
stroke subgroups (with or without perceptual deficits) in the
subgroup analyses.
Group effects were evaluated between values from the
left arm of controls and the affected and less-affected arm
of individuals with stroke. In addition, we evaluated
differences between stroke subgroups (stroke subjects with
and without visuo-perceptual impairment) for movements
made with the more-affected and less-affected arms. To
address the first hypothesis, data from the subgroup of
stroke subjects with visuo-perceptual impairments
performing the task with the less-affected arm (predominant
visuo-perceptual impairment) were compared to controls.
To address the second hypothesis, data from the subgroup
of stroke subjects with no visuo-perceptual impairments
using the affected arm (predominant sensorimotor
impairment) were compared to controls.
Spearman rank order correlations (rho) were used to
identify relationships between the grasp-height effect
(measured as grasp height difference between the 35 and
70% targets) and clinical variables of sensation, spasticity
and motor impairment for the affected arm and cognition
and visuo-perceptual impairment for the less-affected arm.
Correlations with visuo-perceptual impairments were only
tested for the whole stroke group.
Results
Clinical characteristics of individuals with stroke are
shown in Table 1. All but one participant in each group
were right-hand dominant. There were no differences in
age (p = 0.377) or sex (p = 0.078) between participants
with stroke and controls. No clear difference in the lesion
location was found between individuals with or without
visuo-perceptual impairment due to stroke. MoCA scores
were significantly lower in the stroke subgroup with
visuoperceptual impairment compared to those without
impairment (p = 0.007). Since grasp heights and other kinematic
measures did not differ between the left and right arms of
control subjects, the left arm of controls was used for all
comparisons with persons with stroke.
Reach‑to‑grasp kinematics in stroke and healthy controls
Movements of the affected arm in individuals with
stroke, regardless of the presence of visuo-perceptual
impairments, were significantly slower (F2,48 = 5.6–7.9,
p < 0.05, Fig. 2a) and had lower peak velocities (affected
arm 1335–1597 mm/s, less-affected arm 1789–1996 mm/s,
controls 1769–2083 mm/s, F2,48 = 5.0–7.4, p < 0.05)
compared to the less-affected arm and left arm of controls.
Individuals with stroke also used more axial trunk rotation
(F2,48 = 3.4–4.1, p < 0.05), less shoulder horizontal
adduction (F2,48 = 5.7–8.5, p < 0.05) and less elbow extension
(F2,48 = 6.5–10.1, p < 0.05) of the affected arm at the time
of grasping compared to controls (Fig. 2b–d). Kinematics
of the less-affected arm of stroke subjects, regardless of
the presence of visuo-perceptual impairments, did not
differ from those of controls except for shoulder horizontal
adduction for the 35% target height in the subgroup with
visuo-perceptual impairments (Fig. 2).
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Fig. 2 Histograms of mean (SD) kinematic variables of the
reach-tomove task for the stroke group, the stroke subgroup with no
visuoperceptual impairments (no VPI), the stroke subgroup with
visuoperceptual impairments (VPI) and the left arm of the healthy control
subjects. Movement time of reaching, arm and trunk angle position
data at the end of the reach phase are shown. Full elbow extension
and horizontal arm abduction laterally in line with the shoulders were
defined as 0°. *p < 0.05 compared to healthy controls
Grasp‑height effect in stroke (whole group) and healthy controls
The initial grasp height at the home position varied with
target platform height both in individuals with stroke (affected
arm and non-affected arm) and in controls (F3,48 = 105,
p = 0.0001) such that a higher grasp on the plunger shaft was
used for moves to lower target heights, and a grasp closer
to the base of the plunger was used for moves to higher
target heights. Individuals with stroke varied their grasp
height according to the grasp-height effect, but to a lesser
degree compared to controls. The overall effects are
illustrated in Fig. 3a. Since there were no differences in mean
grasp heights in any group for the 70 and 80% target
platform heights (p > 0.025), linear pairwise plots were
constructed for grasp height values between the 35 and 70%
target heights. The slope of this relationship was lower for
the whole stroke group when using their less-affected arm
compared to arms of healthy subjects (p = 0.009; Fig. 3a;
Table 2B). The absolute grasp heights used for moves to
each target platform height and the differences in grasp
heights between target heights are listed for all groups in
Table 2.
The mixed models analysis indicated a significant
interaction between target platform heights and groups
(affected and less-affected arms in stroke, left arms in
controls; F6,48 = 3.93, p = 0.003; Fig. 3a). Age (p = 0.49), sex
(p = 0.70), cognitive impairment (p = 0.94), lesion side
(p = 0.80) and trial order (p = 0.92) were not significant
when added to the mixed analysis model.
Visuo‑perceptual impairments and grasp‑height effect
Similar to the whole group analysis, there was a significant
interaction between target height and group for the four
stroke subgroups and the left arms in controls (Fig. 3b;
F12,45 = 2.86, p = 0.005). Slopes of grasp heights between
the 35 and 70% target platform heights were lower for the
subgroup of stroke subjects with visuo-perceptual
impairments compared to controls when the task was either
Fig. 3 Linear relationships, plotted as slopes, of grasp height
values for 35 and 70% target platform heights for a the less-affected
(n = 17) and affected (n = 17) arms of subjects with stroke, and for
b subgroups of stroke subjects with (VPI, n = 7) and without
visuoperceptual impairment (no VPI, n = 10) together with the left arm
of healthy controls (control, n = 17). Significant differences between
stroke groups/subgroups compared to controls are indicated
performed with the less-affected (p = 0.0009) or the affected
arm (p = 0.005; Fig. 3b; Table 2B). Thus, in line with the
first hypothesis, the grasp-height effect was decreased in
persons with stroke who had visuo-perceptual deficits compared
to healthy controls. This effect was observable in both arms,
although the slope was decreased most when the task was
performed with the less-affected arm.
Motor impairments and grasp‑height effect
According to the second hypothesis, the level of motor
impairment was expected to influence the grasp height
primarily in stroke subjects without visuo-perceptual deficits
performing the task with the affected arm. In this subgroup,
absolute grasp heights used for each target condition did
not differ from controls (Table 2A). The slopes for grasp
heights between the 35 and 70% target platform heights
were not different from controls when the task was either
performed with the less-affected (p = 0.21) or affected arm
(p = 0.65; Table 2B; Fig. 3b). Thus, in individuals without
visuo-perceptual impairments, the grasp-height effect was
not different from controls irrespective of which arm was
used to perform the task.
Grasp‑height effect and other clinical impairments
Sensory, spasticity and motor impairments after stroke
were not correlated with the grasp-height effect for affected
arms and cognitive impairments were not correlated with
Controls (n = 17)
344.7 (59.5)
180.4 (63.9)
144.3 (49.4)
123.4 (32.0)
Controls (n = 17)
VPI visuo-perceptual impairment
* p < 0.025, ** p < 0.01, *** p < 0.001 compared to controls
83.1*** (72.8) 45.9*** (55.7) 110.0* (82.4)
158.7 (83.0) 112.2** (68.2) 189.6 (92.1)
162.4* (84.8) 133.0** (94.2) 182.9 (87.9)
75.5 (64.2) 66.3 (18.6) 79.6 (80.1)
3.7 (22.3) 20.8 (48.9) −6.8 (28.7)
164.4 (67.2)
200.4 (67.6)
221.3 (56.1)
36.0 (61.0)
20.9 (33.0)
the grasp-height effect for less-affected arms in the whole
group and for subgroups with or without visuo-perceptual
impairments. In the whole stroke group, the visuo-perceptual
impairments were not correlated with the grasp-height effect.
Discussion
This study investigated whether and to what extent
visuoperceptual and motor deficits due to stroke influence motor
planning and execution in sequential reaching and moving
an object to different heights in the arm workspace.
Movement planning of this two-sequence task was reflected in the
relationship between the initial grasp height on the plunger
shaft and the final position of the target platform to which
the plunger was to be moved. In young healthy adults, a
linear relationship between the grasp height and the target
platform height has been observed
(Cohen and Rosenbaum
2004; Rosenbaum et al. 2006)
. This relationship, described
as the grasp-height effect, represents an efficiency constraint
in movement planning, in which the initial grasp height is
modulated with respect to the final goal of the task
(Rosenbaum et al. 2012).
The grasp-height effect was present in all groups and
subgroups, but the extent of this effect was decreased in the
subgroup of stroke subjects with visuo-perceptual deficits.
The decrease in grasp-height effect was present irrespective
of the arm used for the task, but it was most evident when
the task was performed with the less-affected non-paretic
arm, for which the motor impairments did not interfere with
movement planning and performance. In the stroke
participants with visuo-perceptual deficits, a lower grasp height
was used for moving the plunger to the lowest target height
and a higher one was used for all other target heights
compared to controls (Table 2). In other words, the variation
in grasp height for moving the plunger to different target
heights was smaller in this group.
Despite the high prevalence of visuo-perceptual deficits
in patients with stroke, it is unclear how these deficits might
affect motor planning and execution. Studies investigating
perceptuo-motor coupling in clinical populations are few
and visuo-perceptual deficits are generally not reported.
The strength of the present study is the use of an objective
and sensitive method (i.e., kinematics) for determining the
exact position of the grasp on the object and to control for
whether the existing movement impairments influenced the
grasp-height effect. Furthermore, testing both the affected
and less-affected arms of the stroke subjects allowed us to
identify the grasp-height effect separately for those with
sensorimotor or visuo-perceptual impairments. Our findings
that visuo-perceptual impairments, particularly observable
for movements not confounded by motor deficits, influenced
the grasp-height effect, add valuable new information about
deficits in movement planning and execution in clinical
populations. The study also adds new knowledge of
movement planning in individuals with more subtle
visuo-perceptual impairments, since those with visual neglect were
not included.
The end-state comfort effect during a bar rotation task
with the less-affected arm was decreased in adults with
visual agnosia and cerebral palsy
(Craje et al. 2009; Dijkerman
et al. 2009)
. Individuals with stroke and visuo-spatial
disorders affecting the perception of line orientations, showed a
decreased end-state comfort effect while performing a
twosequence bar rotation task with the ipsilesional arm
(Hermsdorfer et al. 1999). However, this decreased effect may have
been partly accounted for by the presence of neglect and
hemianopia in their study participants. In contrast, in
individuals with stroke and apraxia, grip selection was
similar to controls, although movement execution was slower
and uncoordinated
(Hermsdorfer et al. 1999)
. In our study,
persons with neglect were excluded, but a decreased
graspheight effect was still observed in individuals with
visuoperceptual impairments, which implies that more subtle
visuo-perceptual deficits may also influence grip selection
and the end-state comfort effect.
The end-state comfort effect was also decreased in
older adults between 71 and 80 years compared those aged
60–70 years, in whom the end-state comfort effect was
comparable to young adults
(Wunsch et al. 2015)
. An increase
in task complexity, requiring bimanual manipulation was
also shown to decrease the end-state comfort effect in older
adults
(Wunsch et al. 2015)
. These authors concluded that
the decrease in the older group may be associated with
reduced cognitive capabilities. In the current study, the mean
age of the control and stroke groups was 64 and 60 years,
respectively, and the task was unilateral. Thus, the
cognitive demand for the plunger transport task was relatively
low and the risk of possible decline related to age was
relatively small. In addition, neither age nor cognitive
impairment significantly influenced the grasp-height effect in the
current study. Increased demand on precision has also been
suggested to influence the end-state comfort effect such that
a more comfortable hand or grasp position is selected in the
phase in which the highest precision is needed
(Kunzell et al.
2013; Rosenbaum et al. 2012)
. However, this was unlikely
to have influenced our results since in our task, the
requirements for precision were low, as the target platform was
larger than the base of the plunger and the plunger itself had
a steady base.
Anticipatory movement planning of functional
reach-tograsp movements can be investigated in several ways. In the
current study, the grasp-height effect was used to gain insight
into motor planning and action selection in accordance with
the end-state comfort effect. Tasks requiring a larger degree
of object rotation (i.e., 180° rotations) have been suggested
to be more sensitive to the end-state comfort effect in healthy
populations
(Wunsch et al. 2013)
. On the other hand, when
the hand-orientation and grasp-height effect were
investigated together in the same task in young adults, end-state
comfort was prioritized both for the grasp orientation and
height
(Cohen and Rosenbaum 2011)
. Since 180°
rotations may be challenging for individuals with stroke due
to motor deficits, we chose to study the end-state effect of
grasp height in this first study with individuals after stroke.
End-state comfort based on orienting a dowel and rotating a
card has also been used to evaluate treatment effects on the
paretic arm in persons with chronic stroke
(Tan et al. 2012)
.
Persons with stroke used a grasp posture consistent with the
end-state comfort effect in most trials (68%), but less
frequently than controls (91%). Tan et al. (2012) also reported
that the number of trials consistent with the end-state
comfort effect increased after constraint-induced movement
therapy. Whether the diminished end-state comfort effect was a
result of impaired motor planning or a combined effect of
motor impairment and planning deficits, however, cannot be
determined since the task was only performed with the more
affected upper limb. Thus, the motor impairment may have
obscured possible effects of visuo-perceptual deficits. In our
study, visuo-perceptual deficits, and not motor impairments,
accounted for deficits in motor planning in our subgroup
of stroke subjects. This is supported by findings that the
grasp-height effect was decreased in all stroke subjects with
visuo-perceptual impairments regardless of which arm was
used (paretic or non-paretic) and that the grasp-height effect
was preserved in stroke subjects without visuo-perceptual
deficits when using the more-affected arm.
A growing body of research suggests hemispheric
specialization for different aspects of movement
(Haaland
et al. 2004; Mani et al. 2013; Sainburg and Schaefer 2004;
Schaefer et al. 2007)
. Hemisphere-specific effects in
endpoint control in reaching with the paretic arm were found
in individuals with stroke after right but not left brain
damage (Stewart et al. 2014). These differences could
not be explained by age, time post-stroke, motor function
or apraxia, but instead, may be related to differences in
visual-motor processing, since visual perception deficits,
assessed using the MVPT, were larger in the right brain
damaged group
(Stewart et al. 2014)
. The right hemisphere
has been suggested to play a dominant role in processing
visuo-spatial effects of goal-directed movements
(Hermsdorfer et al. 1999)
, whereas each hemisphere may be
specialized for different aspects of task execution
(Mani et al.
2013; Mutha et al. 2012; Sainburg and Schaefer 2004)
.
Studies in individuals with stroke are, however, few and
future studies with selected groups are warranted. In the
current study, the side of the lesion did not influence the
grasp-height effect when added to the analyses, which
partly may be related to the small sample size and the
low task difficulty. Larger studies directly investigating
hemispheric differences including kinematic analysis and
taking visuo-perceptual deficits into account may
provide more accurate information regarding hemispheric
lateralization.
Results from the subgroup analysis should be interpreted
with caution, partly because of the small sample sizes, and
partly because other impairments, such as sensory
impairments or apraxia not observed during clinical assessments
(Randerath et al. 2009)
, may also have affected the
graspheight effect. The grasp-height effect showed, however, no
correlations with sensory impairments, spasticity or
cognitive impairment. It is recognized that deficits in different
MVPT domains including the ability to discriminate and
recall dominant features of an object, distinguish it from
the background, orient one’s body in space and perceive the
object position in relation to oneself and to other objects,
might all have affected movement planning of functional
reaching in the current study. However, since individual
domains of visual perception of the MVPT have not been
validated, the results cannot be related to specific perceptual
domains, which is a limitation of the study. Future studies
should include a more specific and comprehensive
assessment of perceptual and cognitive impairments, preferably
together with lesion analysis
(Randerath et al. 2010)
, to help
identify the relationships between these impairments and
motor behavior more precisely. The results of this study can
only be applied to individuals with moderate to mild motor
impairment who are in the chronic stage of stroke and
independent in standing during functional tasks. In the current
study, only linear modeling for grasp height data was used
and future studies should consider data collection from a
larger number of possible target heights and nonlinear
modeling for investigating the grasp-height effect both in healthy
and clinical populations.
Visuo-perceptual deficits in individuals with stroke
impacted planning and selection of movements of a
twosequence functional task. This suggests that in clinical
settings, patients should practice tasks involving planning over
two steps that require different hand orientations, in order to
facilitate improvement of perceptuo-motor skills.
Furthermore, to develop the ability to modulate the grasp according
to object affordances, practice of reaching tasks to different
locations in the arm workspace within a training session
is recommended. An increased understanding of
underlying motor control processes would facilitate development
and implementation of effective interventions to improve
perceptuo-motor skills in individuals with stroke.
Acknowledgements Thanks to all participants of the study, R.
Guberek, PT, M.Sc., for assistance with participant recruitment at the
Center for Interdisciplinary Research in Rehabilitation (CRIR), McGill
University and Jewish Rehabilitation Hospital, and K. Petersson for
statistical help.
Compliance with ethical standards
Funding MAM was supported by Swedish Brain Foundation, Konrad
and Helfrid Johanssons Research Foundation at Gothenburg University
and Reneé Eanders Foundation. MFL holds a Canada Research Chair
in Motor Recovery and Rehabilitation.
Conflict of interest The authors declare that they have no conflict
of interest.
Open Access This article is distributed under the terms of the
Creative Commons Attribution 4.0 International License (http://
creativecommons.org/licenses/by/4.0/), which permits unrestricted
use, distribution, and reproduction in any medium, provided you give
appropriate credit to the original author(s) and the source, provide
a link to the Creative Commons license, and indicate if changes
were made.
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